A Genomic Analysis of Factors Driving lincRNA Diversification: Lessons from Plants

Transcriptomic analyses from across eukaryotes indicate that most of the genome is transcribed at some point in the developmental trajectory of an organism. One class of these transcripts is termed long intergenic noncoding RNAs (lincRNAs). Recently, attention has focused on understanding the evolut...

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Main Authors: Andrew D. L. Nelson, Evan S. Forsythe, Upendra K. Devisetty, David S. Clausen, Asher K. Haug-Batzell, Ari M. R. Meldrum, Michael R. Frank, Eric Lyons, Mark A. Beilstein
Format: Article
Language:English
Published: Oxford University Press 2016-09-01
Series:G3: Genes, Genomes, Genetics
Subjects:
Online Access:http://g3journal.org/lookup/doi/10.1534/g3.116.030338
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author Andrew D. L. Nelson
Evan S. Forsythe
Upendra K. Devisetty
David S. Clausen
Asher K. Haug-Batzell
Ari M. R. Meldrum
Michael R. Frank
Eric Lyons
Mark A. Beilstein
author_facet Andrew D. L. Nelson
Evan S. Forsythe
Upendra K. Devisetty
David S. Clausen
Asher K. Haug-Batzell
Ari M. R. Meldrum
Michael R. Frank
Eric Lyons
Mark A. Beilstein
author_sort Andrew D. L. Nelson
collection DOAJ
description Transcriptomic analyses from across eukaryotes indicate that most of the genome is transcribed at some point in the developmental trajectory of an organism. One class of these transcripts is termed long intergenic noncoding RNAs (lincRNAs). Recently, attention has focused on understanding the evolutionary dynamics of lincRNAs, particularly their conservation within genomes. Here, we take a comparative genomic and phylogenetic approach to uncover factors influencing lincRNA emergence and persistence in the plant family Brassicaceae, to which Arabidopsis thaliana belongs. We searched 10 genomes across the family for evidence of > 5000 lincRNA loci from A. thaliana. From loci conserved in the genomes of multiple species, we built alignments and inferred phylogeny. We then used gene tree/species tree reconciliation to examine the duplication history and timing of emergence of these loci. Emergence of lincRNA loci appears to be linked to local duplication events, but, surprisingly, not whole genome duplication events (WGD), or transposable elements. Interestingly, WGD events are associated with the loss of loci for species having undergone relatively recent polyploidy. Lastly, we identify 1180 loci of the 6480 previously annotated A. thaliana lincRNAs (18%) with elevated levels of conservation. These conserved lincRNAs show higher expression, and are enriched for stress-responsiveness and cis-regulatory motifs known as conserved noncoding sequences (CNSs). These data highlight potential functional pathways and suggest that CNSs may regulate neighboring genes at both the genomic and transcriptomic level. In sum, we provide insight into processes that may influence lincRNA diversification by providing an evolutionary context for previously annotated lincRNAs.
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spelling doaj.art-a4d252df15e847b5bac1b0ed10d2dd052022-12-21T18:36:17ZengOxford University PressG3: Genes, Genomes, Genetics2160-18362016-09-01692881289110.1534/g3.116.03033820A Genomic Analysis of Factors Driving lincRNA Diversification: Lessons from PlantsAndrew D. L. NelsonEvan S. ForsytheUpendra K. DevisettyDavid S. ClausenAsher K. Haug-BatzellAri M. R. MeldrumMichael R. FrankEric LyonsMark A. BeilsteinTranscriptomic analyses from across eukaryotes indicate that most of the genome is transcribed at some point in the developmental trajectory of an organism. One class of these transcripts is termed long intergenic noncoding RNAs (lincRNAs). Recently, attention has focused on understanding the evolutionary dynamics of lincRNAs, particularly their conservation within genomes. Here, we take a comparative genomic and phylogenetic approach to uncover factors influencing lincRNA emergence and persistence in the plant family Brassicaceae, to which Arabidopsis thaliana belongs. We searched 10 genomes across the family for evidence of > 5000 lincRNA loci from A. thaliana. From loci conserved in the genomes of multiple species, we built alignments and inferred phylogeny. We then used gene tree/species tree reconciliation to examine the duplication history and timing of emergence of these loci. Emergence of lincRNA loci appears to be linked to local duplication events, but, surprisingly, not whole genome duplication events (WGD), or transposable elements. Interestingly, WGD events are associated with the loss of loci for species having undergone relatively recent polyploidy. Lastly, we identify 1180 loci of the 6480 previously annotated A. thaliana lincRNAs (18%) with elevated levels of conservation. These conserved lincRNAs show higher expression, and are enriched for stress-responsiveness and cis-regulatory motifs known as conserved noncoding sequences (CNSs). These data highlight potential functional pathways and suggest that CNSs may regulate neighboring genes at both the genomic and transcriptomic level. In sum, we provide insight into processes that may influence lincRNA diversification by providing an evolutionary context for previously annotated lincRNAs.http://g3journal.org/lookup/doi/10.1534/g3.116.030338lincRNABrassicaceaecomparative genomicsevolutiontranscriptomics
spellingShingle Andrew D. L. Nelson
Evan S. Forsythe
Upendra K. Devisetty
David S. Clausen
Asher K. Haug-Batzell
Ari M. R. Meldrum
Michael R. Frank
Eric Lyons
Mark A. Beilstein
A Genomic Analysis of Factors Driving lincRNA Diversification: Lessons from Plants
G3: Genes, Genomes, Genetics
lincRNA
Brassicaceae
comparative genomics
evolution
transcriptomics
title A Genomic Analysis of Factors Driving lincRNA Diversification: Lessons from Plants
title_full A Genomic Analysis of Factors Driving lincRNA Diversification: Lessons from Plants
title_fullStr A Genomic Analysis of Factors Driving lincRNA Diversification: Lessons from Plants
title_full_unstemmed A Genomic Analysis of Factors Driving lincRNA Diversification: Lessons from Plants
title_short A Genomic Analysis of Factors Driving lincRNA Diversification: Lessons from Plants
title_sort genomic analysis of factors driving lincrna diversification lessons from plants
topic lincRNA
Brassicaceae
comparative genomics
evolution
transcriptomics
url http://g3journal.org/lookup/doi/10.1534/g3.116.030338
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